Abstract
Direction selectivity is a prominent feature of single units in the central visual pathway of cat and monkey. Various mechanisms have been proposed for the generation of this property. Experimental evidence suggests that intracortical inhibition is a major factor contributing to direction selectivity.
We have developed a one-dimensional computer model for direction selective simple cells in the visual cortex under two basic assumptions:
1) Inhibition is exerted upon a cortical cell by neighboring cells from either side within a retinotopic array, 2) The relative strength of inhibition from both neighbors can be varied, interneurons always having larger time constants than the simple cells. Summation in the model is linear, but is followed by an essential non-linearity. ON- and/or OFF-center cells of the sustained type (X-cells) are used as an input to the simple cells.
The computer simulation demonstrates that various subtypes of direction-selective simple cells in area 17, as described by Schiller et al. (1976), can be generated by different amounts of inhibition asymmertry, different delays and by different spatial arrangements of the input. Only one type of input (ON or OFF) is required to generate direction selectivity, but a greater variety of cell subtypes is created by combining both. Length-summation, contributing to orientation selectivity, was not considered in this one-dimensional model.
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References
Barlow HB, Levick WR (1965) The mechanism of directionally selective units in rabbit's retina. J Physiol 178:477–506
Benevento LA, Creutzfeldt OD, Kuhnt U (1972) Significance of intracortical inhibition. Nature 283:124–126
Bishop PO, Coombs JS, Henry GH (1971) Responses to visual contours: Spatiotemporal aspects of excitation in the receptive fields of simple striate neurones. J Physiol 219:625–657
Bullier J, Henry GH (1979) Neural path taken by afferent streams in striate cortex of the cat. J Neurophysiol 42:1271–1281
Bullier J, Mustari M, Henry GH (1982) Receptive field transformations between LGN-neurons and S-cells of cat striate cortex. J Neurophysiol 47:417–438
Cleland BG, Dubin MW, Levick WR (1971) Sustained and transient neurones in the cat's retina and LGN. J Physiol 217:473–496
Creutzfeldt OD, Ito M (1968) Functional synaptic organization of primary visual cortex neurons in the cat. Exp Brain Res 6:324–352
Dreher B, Sanderson KJ (1973) Receptive field analysis: responses to moving visual contours by single laterale geniculate neurones in the cat. J Physiol 234:95–118
Emerson RC, Gerstein GL (1977) Simple striate neurons in the cat. II. Mechanisms underlying directional asymmetry and directional selectivity. J Neurophysiol 40:136–155
Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187:517–552
Ferster D (1986) Orientation selectivity of synaptic potentials of cat primary visual cortex. J Neurosci 6:1284–1301
Ganz L (1984) Visual cortical mechanisms responsible for direction selectivity. Vision Res 24:3–11
Goodwin WA, Henry GH, Bishop PO (1975) Direction selectivity of simple striate cells. Properties and mechanism. J Neurophysiol 38:1500–1523
Hassenstein B, Reichardt W (1956) Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Z Naturforsch 11b:513–524
Heggelund P (1981) Receptive field organization of simple cells in cat striate cortex. Exp Brain Res 42:89–98
Heggelund P (1986) Quantitative studies of the discharge fields of single cells in cat striate cortex. J Physiol 373:277–292
Henry GH, Dreher B, Bishop PO (1974) Orientation specificity of cells in cat striate cortex. J Neurophysiol 37:1394–1409
Hoffmann KP, Stone J (1971) Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties. Exp Brain Res 32:460–466
Hubel DH, Wiesel TN (1959) Receptive fields of single neurones in the cat's striate cortex. J Physiol 148:574–591
Hubel DH, Wiesel TN (1961) Integrative action in the cat's lateral geniculate body. J Physiol 155:385–398
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160:106–154
Hubel DH, Wiesel TN (1974) Uniformity of monkey striate cortex: a parallel relationship between field size, scatter and magnification factor. J Comp Neurol 158:295–306
Kuffler SW (1953) Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16:37–68
LeVay S, McConnell SK (1982) ON and OFF layers in the lateral geniculate nucleus of the mink. Nature 300:350–351
Marr D, Ullman S (1981) Directional selectivity and its use in early visual processing. Proc R Soc London 211:151–180
Movshon JA (1975) The velocity tuning of single units in cat striate cortex. J Physiol 249:445–468
Movshon JA, Thompson ID, Tolhurst DJ (1978) Spatial summation in the receptice fields of simple cells in the cat's striate cortex. J Physiol 283:53–77
Mullikin WH, Jones JP, Palmer LA (1984) Receptive-field properties and laminar distribution of x-like and y-like simple cells in cat area 17. J. Neurophysiol 52:350–371
Mustari M, Bullier J, Henry GH (1982) Comparison of response properties of three types of monosynaptic simple cell in cat striate cortex. J Neurophysiol 42:439–454
Orban GY (1984) Neuronal operations in the visual cortex. Springer, Berlin Heidelberg New York
Palmer LA, Davis TL (1981) Receptive-field structure in cat striate cortex. J Neurophysiol 46:260–276
Peichl L, Wässle H (1979) Size scatter and coverage of ganglion cell receptive field centers in the cat retina. J Physiol 291:117–141
Peterhans E, Bishop PO, Camarda RM (1985) Direction selectivity of simple cells in cat striate cortex to moving light bars. I. Relation to stationary flashing bar and moving edge responses. Exp Brain Res 57:512–522
Poggio T, Reichardt W (1973) Considerations on models of movement detection. Kybernetik 13:223–227
Reichardt W (1961) Autocorrelation, a principle for evaluation of sensory information by the central nervous system. In: Rosenblith WA (ed) Principles of sensory communications, Wiley, New York, pp 303–317
Reichardt W, Poggio T (1976) Visual control of orientation behaviour in the fly. Part II. Quart Rev of Biophysics 9, 3:377–438
Richter J, Ullman S (1982) A model for the temporal organization of X- and Y-type receptive fields in the primate retina. Biol Cybern 43:127–145
Schiller PH (1982) Central connections of the retinal ON and OFF pathways. Nature 297:580–583
Schiller PH, Finlay BL, Volman SF (1976) Quantitative studies of single-cell properties in monkey striate cortex. I–V. J Neurophysiol 39:1288–1374
Schiller PH, Sandell JH, Maunsell JHR (1986) Functions of the ON and OFF channels of the visual system. Nature 322:824–825
Sherk H, Horton JC (1984) Receptive field properties in the cat's area 17 in the absence of ON-center geniculate input. J Neurosci 4:381–393
Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol 250:305–329
Sillito AM (1977) Inhibitory processes underlying the directional specifity of simple, complex and hypercomplex cells in the cat's visual cortex. J Physiol 271:699–720
Singer W, Tretter F, Cynader M (1975) Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. J. Neurophysiol 18:1080–1098
Steinberg RH, Reid M, Lacy PL (1973) The distribution of rods and cones in the retina of the cat. J Comp Neurol 148:229–248
Stevens JK, Gerstein GL (1976) Spatiotemporal organization of cat lateral geniculate receptive fields. J Neurophysiol 39:213–238
Vidyasagar TR, Urbas JV (1982) Orientation sensitivity of cat LGN neurons with and without inputs from visual cortical areas 17 and 18. Exp Brain Res 46:157–169
Vitanova L, Glezer V, Gauselman V (1985) On the mechanisms underlying appearance of responses to movement, directional sensitivity and velocity tuning of the cat's striate cortical neurons. Biol Cybern 52:237–246
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Ruff, P.I., Rauschecker, J.P. & Palm, G. A model of direction-selective “simple” cells in the visual cortex based on inhibition asymmetry. Biol. Cybern. 57, 147–157 (1987). https://doi.org/10.1007/BF00364147
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DOI: https://doi.org/10.1007/BF00364147